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 Table of Contents  
ORIGINAL ARTICLES
Year : 2022  |  Volume : 22  |  Issue : 3  |  Page : 168-178

Vascular access thrombosis among end-stage renal disease patients with acute COVID19 infection (a retrospective cohort study)


1 Department of Vascular Surgery, Faculty of Medicine, Helwan University, Cairo, Egypt
2 Department of Internal Medicine, Faculty of Medicine, Alexandria University, Alexandria, Egypt
3 Department of Vascular Surgery, Faculty of Medicine, Alexandria University, Alexandria, Egypt
4 Department of Chemical and Clinical Pathology, Faculty of Medicine, Alexandria University, Alexandria, Egypt
5 Department of Community Medicine, Faculty of Medicine, Alexandria University, Alexandria, Egypt
6 Department of Vascular Surgery, Faculty of Medicine, Kafr Elsheikh University, Kafr Elsheikh, Egypt

Date of Submission20-Dec-2021
Date of Acceptance30-Dec-2021
Date of Web Publication22-Jul-2022

Correspondence Address:
Dr. Rasha I Gawish
37 Ismail Serry St., Smouha, Alexandria, Postal Code: 21648
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jesnt.jesnt_39_21

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  Abstract 

Background According to studies, coronavirus disease 2019 (COVID19) infection is linked to an elevated risk of venous thromboembolism (TE). The frequencies of overall COVID19 thrombotic events and the influence of TE on COVID19 mortality, however, are unknown. Although respiratory symptoms are the most common symptom of the disease, evidence is growing suggesting that it is linked to coagulation system malfunction, which puts patients at risk for venous and arterial TE and higher mortality as well. Materials and methods A retrospective cohort study was conducted on 50 end-stage renal disease patients on maintenance hemodialysis (25 patients with confirmed COVID19 infection and 25 patients without COVID19 infection) to determine the incidence of vascular access thrombosis among patients with COVID19 during a 3-month period. Risk factors for mortality and severity were considered as secondary outcomes. Patients with previous history of vascular access dysfunction were excluded from the study. Results In all, 24% of COVID19-positive patients (n=6) developed vascular access thrombosis during 3 months of follow-up while no one of the COVID19-negative patient developed access thrombosis. The incidence of vascular access thrombosis was statistically higher in the COVID19 positive group (p value < 0.022). The incidence of vascular access thrombosis was significantly can u please add this part : increased in patients who had lymphopenia, elevated LDH, also it was more common in patients who needed mechanical ventilation and who had severe diseaseConclusion The incidence of vascular access thrombosis was statistically higher in the COVID19 positive group (p value < 0.022). The incidence of vascular access thrombosis was significantly can u please add this part: increased in patients who had lymphopenia, elevated LDH, also it was more common in patients who needed mechanical ventilation and who had severe disease.

Keywords: COVID19, ESRD, vascular access thrombosis


How to cite this article:
Elmahdi AM, Gawish RI, Shalaan WE, Eldin MG, Gamal NA, Mabrouk MH. Vascular access thrombosis among end-stage renal disease patients with acute COVID19 infection (a retrospective cohort study). J Egypt Soc Nephrol Transplant 2022;22:168-78

How to cite this URL:
Elmahdi AM, Gawish RI, Shalaan WE, Eldin MG, Gamal NA, Mabrouk MH. Vascular access thrombosis among end-stage renal disease patients with acute COVID19 infection (a retrospective cohort study). J Egypt Soc Nephrol Transplant [serial online] 2022 [cited 2022 Dec 4];22:168-78. Available from: http://www.jesnt.eg.net/text.asp?2022/22/3/168/351712



Authors’ contributions: W.E.S., M.H.M., and A.M.E. formulated the hypothesis, participated in data collection and analysis, and revised the manuscript. N.A.G. determined the sample size and performed the statistical analysis. M.A.G.E. participated in data collection and supervised the results of the laboratory investigations. R.I.G. participated in data collection and analysis and wrote the initial manuscript. All the authors revised the final manuscript. The manuscript has been read and approved by all authors. The requirements for authorship as stated earlier in this document have been met, and each author believes that the manuscript represents honest work.


  Introduction Top


Severe acute respiratory syndrome coronavirus 2 is a coronavirus that produces a severe respiratory infection and is linked to a high proportion of hospital and intensive care unit (ICU) admissions, as well as a high mortality rate [1,2]. Common complications include shock, secondary bacterial infections, and acute cardiac injury [3].

Coronavirus disease 2019 (COVID19) can lead to systemic viral infection, hypercoagulable state, inflammatory response, increased incidence of noninvasive or invasive mechanical ventilation, immobility, and prolonged ICU stay. In respiratory and other intensive care settings, previous studies demonstrated an elevated risk of deep vein thrombosis, venous thromboembolism, and possible pulmonary embolism [1].

End-stage renal disease (ESRD) patients are more susceptible to COVID19 infection than the general population, owing to a weakened immune system and frequent visits to healthcare institutions. The risk of COVID19-related complications in ESRD patients is still unclear [4,5].

The aim of the study was to determine the incidence of vascular access thrombosis in ESRD patients with COVID19 infection and associated risk factors


  Materials and methods Top


Study design and population

Fifty ESRD patients were enrolled between August 2021 and October 2021 (25 patients with confirmed COVID19 infection and 25 patients without COVID 19 infection). The patients were maintained on 3 times weekly regimen of standard low flux hemodialysis (HD) sessions, 4 h for each session for at least 6 months, and the patients were enrolled from 3 different HD centers.

Ethical approval

The study was approved by the Ethical approval has been taken (IRB NO: 00012098) and was performed in accordance with the 1964 Helsinki Declaration and its later amendments.

Outcomes

Primary outcomes

The primary outcome was to determine the incidence of vascular access thrombosis (arteriovenous fistula (AVF)–arteriovenous graft (AVG)) in maintenance HD (MHD) patients with COVID19 infection and associated risk factors.

Secondary outcomes

The secondary outcome was to determine the relation between different demographic, clinical, and laboratory parameters with the severity and mortality.

Inclusion criteria

Inclusion criteria was age 18–60 years.

Exclusion criteria

Excluion criteria included patients with active malignancy, autoimmune diseases (systemic lupus erythematosus-antiphospholipid syndrome), known hypercoagulable state, history of clinical or radiological evidence of vascular access dysfunction, patients with vascular access of less than 6 months duration and patients with central venous catheters (tunneled and short term).

Data collection

Demographics, comorbidities, COVID19-related symptoms, severity of illness, the use of anticoagulants, the need for mechanical ventilation, and laboratory tests were collected from the HD center and hospital medical records.

Laboratory parameters

Laboratory parameters included complete blood counts with lymphocyte percents, serum concentrations of creatinine, lactate dehydrogenase (LDH), liver enzymes (aspartate transaminase and alanine transaminase), C- reactive protein (CRP), D-dimer, prothrombin time, partial thromboplastin time (PTT), and international normalized ratio.

COVID19 diagnosis

Confirmation of COVID19 diagnosis was done using a positive reverse transcriptase–polymerase chain reaction (nasopharyngeal swab).

Signs of vascular access dysfunction

The clinical signs were lack of or diminished thrill, as well as the absence or aberrant bruit on auscultation [6]. During the HD session, patients with difficult cannulation or decreased access flow as well as increased venous and/or excessively negative arterial pressures were considered to have vascular access dysfunction. The anastomosis might be pulsatile and sometimes erythematous in some cases.

Access thrombosis was usually suspected based on clinical findings and verified by duplex ultrasonography.

Duplex ultrasound

Examination of the AVF or AVG using B mode Doppler ultrasound was done for patients who showed signs of recent vascular access dysfunction upon physical examination before or during the HD session [7–9]. For superficial vascular imaging, linear array transducers (5–10 MHz) were commonly employed. Curved transducers, on the other hand, were used for deeper vascular imaging, such as the inflow arteries and central veins of the shoulder and neck.

The afferent artery, anastomosis site, and draining veins as far as the subclavian vein were all examined. In both transverse and longitudinal planes, all vessels were evaluated using gray-scale and color images. Detection of wall echo pattern and dilatations, as well as measurement of the vessel’s diameter, was determined. Color images were obtained to assess the direction of blood flow. The presence of echogenic material within the lumen and absent color as well as spectral Doppler signal was detected in thrombosed access.

Hospitalization

Mild COVID19 cases (mild symptoms with normal imaging) did not require hospitalization and received outpatient HD in an isolated territory with separate entry and exit sites. Moderate (abnormal imaging and oxygen saturation more than 92%) and severe cases (oxygen saturation <92%, respiratory rate >30 breaths/min, lung infiltrates >50%, respiratory failure, septic shock, and/or multiorgan failure) were hospitalized.

In severe and critically ill patients, cases were considered negative after 2 negative consecutive reverse transcriptase–polymerase chain reaction results from respiratory samples tested at least 1 day apart.

According to the updated Egyptian Ministry Of Health treatment protocol, all patients got standard COVID19 treatment. Anticoagulants were administered for moderate and severe cases (unfractionated heparin at a dose of 5000 subcutaneous/8 h).

COVID19-negative ESRD patients were identified according to the absence of clinical manifestations in addition to their laboratory investigations.

Statistical analysis of the data

A convenient sample of complete and accurate medical records for 25 ESRD COVID19-positive patients and 25 ESRD COVID19-negative controls was surveyed.

The sample size was calculated using the EPI info statistical software program (developer : CDC. City: Atlanta,GA. Country: USA) with 80% power and 95% confidence level.

The data entered into the computer were examined using the IBM SPSS software package version 20.0. (Armonk, NY, USA: IBM Corporation). The Kolmogorov–Smirnov test was used to ensure that variable distributions were normal, and χ2 test was utilized to examine categorical variable comparisons between groups (Monte Carlo). For normally distributed quantitative variables, Student t-test was used to compare two groups, while Mann–Whitney test was used to compare two groups for not normally distributed quantitative variables.


  Results Top


Between 1 August 2021 and 31 October 2021, 50 ESRD patients on MHD were enrolled (25 with confirmed COVID19 infection and 25 without COVID19 infection).

Demographic data

COVID19-positive patients had a mean age of 46.7 ± 12.1 versus 49.4 ± 6.3 years of the negative patients with no statistically significant difference. In al 76.0% (n=19) of the COVID19-positive patients were males and 24.0% (n=6) were females.

Comorbid conditions

Hypertension (HTN) and diabetes mellitus (DM), respectively, were found in 52.0% (n=13) and 48.0% (n=12) of the COVID19-positive patients versus 44% (n=11) and 36% (n=9) of the negative patients.

Clinical manifestations

Among the COVID19-positive patients, 17 (68.0%) had fever and dry cough and 8 (32.0%) had dyspnea, while the negative patients 2 (8.0%) reported exertional dyspnea ([Table 1]).
Table 1: Comparison between the two studied groups according to demographic and clinical parameters

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Vital signs

The mean temperature in COVID19-positive group was 37.6 ± 0.87 versus 37.0 ± 0.05 in the COVID19 negative and the difference was statistically significant.

The mean systolic blood pressure (BP) in COVID19-negative patients was 135.8 ± 12.3 versus 131.5 ± 17.0 in the positive group. The mean diastolic BP in COVID19-negative patients was 81.96 ± 12.56 versus 82.40 ± 11.0 in the positive group. There was no statistically significant difference between the two groups.

The mean respiratory rate in the COVID19-negative group was 17.4 ± 2.5 versus 21.9 ± 3.2 in the positive group and the difference was statistically significant.

The mean pulse in the COVID19-negative group was 82.84 ± 8.55, while in the COVID19-positive group, it was 89.20 ± 9.25 with a statistically significant difference ([Table 1]).

Laboratory investigations

The mean hemoglobin in the COVID19-negative patients was 9.35 ± 1.05 versus 9.13 ± 1.14 in the positive group (P=0.472).

The mean lymphocyte percent was 32.08 ± 5.55 in the COVID19-negative patients and 10.88 ± 6.75 in the positive patients and the difference was statistically significant. (P<0.001).

The mean CRP in the COVID19-negative group was 18.5 ± 6.48 versus 90.7 ± 28.1 in the positive group (P<0.001).

The mean D dimer in the COVID19-negative group was 323.8 ± 85.6 versus 1712.1 ± 907.3 in the positive group. (P<0.001).

The mean erythrocyte sedimentation rate in the COVID19-negative group was 17.8 ± 4.4 versus 71.6 ± 17.8 in the positive group (P<0.001).

The mean LDH in the COVID-positive group was 352.99 ± 166.75 versus 204.80 ± 46.80 in the COVID19-negative group (P<0.001). Aspartate transaminase and alanine transaminase were also significantly higher in the COVID19-positive group (P 0.005 and <0.001, respectively; [Table 2]).
Table 2: Comparison between the two studied groups according to laboratory investigations

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Management

Mild cases underwent strict home isolation and HD was performed in an isolated territory; personal protective equipment was supplied to all the personnel who dealt with the patients; the mild cases (n=9) received paracetamol and multivitamins. Seven of the moderate cases received steroids and the other four received Remdsevir, steroids, and Tocilizumab. All the severe cases were admitted to the ICU (n=5) and received (Remdsevir, steroids, Tocilizumab, and convalescent plasma). All the severe cases required invasive mechanical ventilation. Five of the 9 mild cases recovered after 7 days and the other 4 recovered after 12 days. As regards the moderate cases, 3 patients were discharged after 9 days, 2 patients after 10 days, and the remaining 6 patients after 12–14 days. All the severe cases required invasive mechanical ventilation and died (n=5).

Comparison between the two studied groups according to AVF thrombosis

Among the COVID19-positive group, 6 out of 25 patients representing 24% developed AVF thrombosis (2 patients developed AVF thrombosis within the first 7 days of illness, the other 4 patients during the second week). while no patients in the COVID19-negative group developed access thrombosis. The incidence of vascular access thrombosis was statistically higher in the COVID19-positive group (P<0.022; [Table 3]).
Table 3: Comparison between the two studied groups according to the incidence of AVF thrombosis

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Salvage procedures could not be performed for severe cases with access thrombosis and the insertion of short-term dialysis catheters was required to resume HD in these patients (n=3). The moderate cases (n=3) who had AVF thrombosis underwent thrombectomy under local anesthesia within 24 h followed by fistulogram; the thrombectomy was successful in only 2 patients and HD was restored through the AVF. In one patient, the thrombectomy failed and a short-term dialysis catheter was used for HD.

There was no significant difference between patients who developed AVF thrombosis and the other COVID19-positive patients as regards age, sex, BMI, HTN, DM, systolic BP, diastolic BP, and hemoglobin concentrations. Patients with AVF thrombosis had significantly lower lymphocyte percents (7.33 ± 0.52 vs. 12.0 ± 7.43) than in patients with no thrombosis (P=0.014). Patients with AVF thrombosis had significantly elevated LDH (512.50 ± 230.99 vs. 302.62 ± 105.33) than in patients with no thrombosis (P=0.025) and prolonged PTT (40.0 ± 7.82 vs. 30.54 ± 8.54) (P=0.024). Also, they had more severe disease and the need for mechanical ventilation was significantly higher among these patients. The mortality among patients who needed mechanical ventilation was 100%. The 5 patients who died had significantly lower lymphocyte percent (7.40 ± 0.55 vs. 11.75 ± 7.32) compared to the patients who survived (P=0.041) and prolonged PTT (41.80 ± 7.22 vs. (30.56 ± 8.31) (P=0.011), elevated LDH (566.0 ± 212.67 vs. 299.74 ± 103.33) (P=0.002), elevated serum glutamic oxaloacetic transaminase and serum glutamic pyruvic transaminase (P=0.007 and 0.004), respectively, while there was no difference between this group and the survivors as regards the other parameters ([Table 4]).
Table 4: Distribution of different parameters among the COVID19-positive group

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As regards the severity among the COVID19-positive group, 5 patients had severe disease (20%) and required mechanical ventilation. Eight (33.3%) of the COVID19-positive patients had mild disease, while 11 (45.8%) of the COVID19-positive patients had moderate disease ([Table 5]).
Table 5: Distribution of the studied cases according to different parameters in positive COVID19 group (n=25)

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  Discussion Top


The medical community has faced extraordinary burden since the advent of the new COVID19.

There is a wide range of COVID19 symptoms as well as outcomes but usually COVID19 tends to be severe in patients with pre-existing comorbidities, with considerable morbidity, increased length of stay in the hospital, ICU admission as well as mortality [10,11]. The internal uremic environment disturbs the immune system and COVID19 frequently has catastrophic consequences for patients on MHD since the risk of infection is higher in HD units [12–15].

The mean age of the COVID19 in the study was 46.7 ± 12 years, which is younger than the mean age in a single-center retrospective cohort study from Pakistan on 43 ESRD patients with COVID19 infection (the mean was 51.4 ± 15.1 years) [16], and also younger than the mean age in a retrospective nationwide study conducted in Qatar [17], which was 56.5 years. Around three-quarters of the infected patients in Qatar study were men. Kazmi and colleagues from Pakistan [16] also demonstrated that males were the most affected, with 25 (58.1%), while females represented 41.9%, which is compatible with the current study findings, which showed that 19 (76.0%) of the COVID19-positive patients were males and 6 (24.0%) were females. This is likely due to the fact that men are more susceptible to infection since they are more socially active, while women are more likely to follow the COVID19 prophylactic procedures [18].

In the same study from Pakistan [16], HTN was seen in 35 (81.4%) of the patients [16]. In our study, 13 (52.0%) of the COVID19-positive patients had HTN, compared to 44% of the COVID19-negative patients. DM was found in 12 (48.0%) of the COVID-positive patients compared to 9 (36%) of the COVID19-negative patients but this difference was not statistically significant. Ghonimi et al. [17] found that HTN (98.7%) and DM (65.7%) were the most commonly associated comorbidities. The most common clinical presentation in their study were fever (57.9%), dry cough (56.6%), and dyspnea (25%), while in the current study the percentage of fever, dry cough, and dyspnea were 68, 68, and 32%, respectively.

The mean lymphocyte percent, CRP and D-dimer were 10.88 ± 6.75, 90.7 ± 28.1, and 1712.1 ± 907.3, respectively, in the COVID19-positive patients compared to 32.08 ± 5.55, 18.5 ± 6.48, and 323.8 ± 85.6 in the COVID19-negative patients (P<0.001).

LDH, serum albumin, and lymphocytic counts were found to be strongly linked with COVID19 outcome in a population of ESRD patients in the same retrospective study from Pakistan [16]. In all, 100% (n=11) of the patients who died showed lymphopenia but non-statistically significant elevated CRP and LDH levels. In our subset of patients, 5 patients of the COVID19-positive group died representing a mortality of 20%; these patients also had statistically significant lymphopenia when compared to the survivors (mean 7.40 ± 0.55 vs. 11.75 ± 7.32, P=0.041).

In a meta-analysis of 78 studies, a positive correlation was found between lymphopenia, LDH of over 250 U/l, leukocytosis of more than 9.5109, and higher mortality [19].

Because lymphopenia is known to alter COVID19 outcomes, it could be used as a prognostic sign in COVID19 disease. Lymphopenia is a critical indicator of the intensity of a cytokine storm [13].

In a Wuhan multi-center study, 41 of the 131 MHD patients died, resulting in a 31.29% mortality [20]. Furthermore, United States, Spain, Italy, and France detected mortality rates of 31.7, 30.5, 52, and 28%, respectively, both in single- and multi-center cohort studies [21–24]. Stefan and Mehedinti from Romania, on the other hand, reported a 19% death rate in their HD group. Also, a multi-center research from Turkey found a 16.2% fatality rate. Our mortality rates are similar to the rates reported from Romania and Turkey but lower than the mortality rates from other countries and this may explained by the younger age of the patients in the current study [14].

Of the 5 patients who died, 3 developed thrombosis of the AVF, and 2 patients died with a functioning fistula. Vascular access thrombosis in the 6 patients occurred early in the course (within 14 days) of the onset of illness that might reflect the relation between the severe viral infection and vascular access thrombosis. Also, the BP was not statistically different among patients with and without AVF thrombosis.

Of the 6 patients who developed AVF thrombosis, 3 had brachiocephalic, 2 patients had brachiobasilic fistula, and 1 patient had radiocephalic fistula. In 1 case, the thrombosis extended to the deep system reaching the axillary vein. Among the COVID19-negative group, there was 1 patient with an AVG while the COVID19-positive group did not include any patient with AVG.

Vascular access thrombosis occurred in 24% of the COVID19-positive patients (n=6) despite prophylactic anticoagulation, and the incidence of thrombosis was significantly increased in patients who had lymphopenia and elevated LDH; also it was more common in patients who needed mechanical ventilation and who had severe disease.

A recent meta-analysis found a high prevalence of venous thromboembolism (reaching about 30% in hospitalized patients with COVID 19), even in patients receiving thromboprophylaxis, and was higher in studies with more than 50% of patients anticoagulated [25].

Obstructive vasculopathy as a cause of thrombosis in COVID19 infection has been a matter of debate. The development of microvascular thrombosis and occlusion has been linked to endothelial damage and autoimmune processes [26,27].

A retrospective cohort study of 185 HD patients at the start of the pandemic found that HD patients have a higher risk of late thrombotic issues after infection with COVID19; COVID19 survivors had a higher incidence of thrombotic events than the non-infected patients after 7 months of follow-up (18.5 vs. 1.9%, P=0.002). However, new vascular access thrombosis was not among the thrombotic occurrences [28].

COVID19-related coagulopathy is thought to result from the acute inflammatory systemic reaction to the virus and its products [29]. The production of cytokines and chemokines like interleukin (IL)-1, IL-6, IL-10, interferon, and macrophage inflammatory proteins 1-alpha and 1-beta is dramatically increased, In patients with concomitant risk factors, this coagulopathy could result in in-situ thrombotic effects [30].

MASP-2, a protease of the lectin complement pathway, has been found to attach directly to the nucleocapsid protein of a number of coronaviruses, including severe acute respiratory syndrome coronavirus 2. This could explain why certain COVID19 patients have complement activation, regardless of whether they are susceptible to abnormal complement responses [31,32]. The viral load and the characteristics of the patient’s immune response are among the factors that affect the progress of COVID19 infection into severe forms characterized by intense cytokine storm, acute respiratory distress syndrome, and microangiopathy [33,34].

None of the six patients who developed AVF thrombosis had a previous thrombotic event. Also, DM and HTN as traditional cardiovascular risk factors were not significantly different between the COVID19-positive and COVID19-negative patients.


  Conclusion Top


The incidence of vascular access thrombosis may be elevated among ESRD with COVID19 infection despite prophylactic anticoagulation. It is also more common in severe cases, patients with lymphopenia, and elevated LDH. The timely implementation of salvage procedures may preserve the vascular access and avoid the need to insert tunneled or short-term dialysis catheters.

Limitations

The small number of patients and the observational nature of the study are the main limitations. Also, the laboratory investigations were not performed according to a regular time frame. Larger prospective studies are needed to confirm these results and to detect whether therapeutic doses of anticoagulants might preserve the vascular access, which is the Achilles tendon for HD without adding significant bleeding risk to the patients.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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